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12
Seed Dispersal of
Mimetic Fruits: Parasitism,
Mutualism, Aposematism
or Exaptation?
Mauro Galetti
Plant Phenology and Seed Dispersal Research Group, Departamento de Ecologia,
Universidade Estadual Paulista (UNESP), CP 199, 13506-900 Rio Claro,
São Paulo, Brazil
Introduction
Fruits and their seed-dispersers are a classic
example of a mutualistic relationship. Seeddispersers benefit from consuming the nutritious tissues surrounding the seeds, whereas
plants benefit from the dispersal of their seeds
away from the competition of the parent to
newly opened habitat and to places away from
the zone of high mortality near the parent
plant (Snow, 1971; Howe and Smallwood,
1982).
Several attributes of fruits, including colour, morphology, seed size, phenology and
pulp chemistry, are considered plant adaptations to enhance the chances of being eaten by
seed-dispersers (van der Pijl, 1982; Janson,
1983; Gautier-Hion et al., 1985). The energy
allocated to produce the pulp or aril represents
a cost to the plant that probably has no purpose
other than to attract seed-dispersers and to protect seeds (Howe, 1993; Mack, 2000). seeddispersers, on the other hand, also incur costs.
Transportation of non-digestible material
(seeds) in their guts and exposure to predators
while feeding ultimately reduce the rate at
which fruit pulp can be processed and
nutrients obtained (McKey, 1975; Levey and
Grajal, 1991; Murray et al., 1993; but see
Witmer, 1998).
As in most mutualistic relationships, some
frugivores and fruiting plants have evolved
strategies to overcome these costs without losing the benefits. For instance, some bird species eat fruit pulp and discard the seeds below
the parent tree, thereby avoiding the costs of
seed ingestion (Levey, 1987). A few plant species have also evolved fruits with no nutritive
rewards, presumably deceiving frugivores into
swallowing their seeds. These plants enjoy the
benefit of dispersal without the cost of pulp
production. One such strategy is to hide small
fruits and seeds among leaves that are ingested
by large herbivores (‘foliage is the fruit’ hypothesis (Janzen, 1984)). Another strategy is to
display colourful seeds resembling fleshy ornithochoric (i.e. bird-dispersed) fruits, so-called
‘mimetic fruits’ (Ridley, 1930; van der Pijl,
1982). The first strategy is relatively well documented (Janzen, 1984; Quinn et al., 1994; Malo
and Suaréz, 1998; Ortmann et al., 1998). The
second strategy, on the other hand, has been
debated since the first monographs on seed dispersal (Ridley, 1930; van der Pijl, 1982), but
©CAB International 2002. Seed Dispersal and Frugivory: Ecology, Evolution and Conservation
(eds D.J. Levey, W.R. Silva and M. Galetti)
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Seed Dispersal of Mimetic Fruits
very few studies have tested the effectiveness of
mimetic fruits in deceiving seed-dispersers
(Peres and van Roosmalen, 1996; Foster and
Delay, 1998).
In a classic sense, mimicry involves matching colours of edible (in Batesian mimicry) or
non-edible species (Müllerian mimicry), to
avoid being eaten by predators (Endler, 1981).
In the case of mimetic fruits, plants produce
seeds that mimic fleshy fruits, thereby facilitating consumption and dispersal of the seed,
which provides no nutritive reward to the bird.
Fruit mimicry systems apparently share many
elements with deceit pollination systems.
These include exploitation of naïve consumers, taking advantage of the exploratory behaviour of the animals and use of the signal ordinarily used by truly rewarding systems (in this
case, nutritious endocarp) (Dafni, 1984).
Taxonomic Affinities of Mimetic
Fruits
Mimetic fruits have been described and discussed by several authors (Ridley, 1930; Corner, 1949; McKey, 1975; van der Pijl, 1982; Williamson, 1982). All of these studies except van
der Pijl (1982) focused particularly on Leguminosae, primarily because its mimetic species
are well known due to their use as jewellery
(Armstrong, 1992). We define a ‘mimetic
fruit’ as a brightly coloured fruit or seed with
no associated pulp or aril: it consequently
does not provide a nutritional reward for
potential seed-dispersers. Although such seeds
are often termed ‘mimetic seeds’, I prefer
‘mimetic fruits’ because the latter terminology
makes explicit the model and, hence, the ecological function of the mimicry. My classification is ecological rather than botanical, since
different species of plants make use of different structures to mimic fruits. Moreover, we
are not concerned with trying to find the probable models for the mimetic fruit, because all
species match colour and display patterns
common among fleshy-fruited bird-dispersed
species.
Mimetic fruits that have a bright visual display are widespread in several non-related
plant families (Colour Plate 1 – see Frontispiece; Table 12.1). At least 21 genera have
mimetic fruits with colourful displays, but this
phenomenon is particularly common in Leguminosae and especially in Mimosoidea. Mimetic
fruits can be found in herbs (Gahnia, Paeonia)
and vines (Rhyncosia, Abrus), but are most common in trees (Abarema, Pithecellobium, Ormosia,
Erythrina, Harpullia) (characteristics and family
names provided in Table 12.1).
The visual display of most mimetic fruits is
a colourful (usually red or red and black or
even blue) or black seed against a contrasting
colourful background such as yellow, red or
orange pods (e.g. Adenanthera pavonina, Abarema spp., Pithecellobium spp., Pararchidendron
pruinosum or Archidendron grandiflorum) or
other structures (such as in Paeonia broteroi
(Colour Plate 1)). In the case of P. broteroi and
other peonies, the non-fertilized ovules are red
and contrast with black fertilized ovules (seeds
with sarcotesta) immersed in a red carpellary
wall (van der Pijl, 1982; C. Herrera, Seville,
2000, personal communication).
Most species with mimetic fruits have long
fruiting seasons, which means that fruits are
available to seed-dispersers for an unusually
long time. Also, the seeds typically have long
dormancy periods and several species are rich
in secondary compounds that may deter pathogens and other seed predators (Table 12.1).
Alkaloids are the main secondary compound
found in mimetic fruits, but saponins and flavonoids also occur (Table 12.1).
One of the most well-known and widespread mimetic species is A. pavonina (Leguminosae, Mimosoidea), which has been introduced worldwide. Van der Pijl (1982) fed
captive barbets (Capitonidae) A. pavonina
seeds, but did not mention whether the seeds
germinated after gut passage. In addition,
Steadman and Freifeld (1999) found six seeds
of A. pavonina in the crop of the purple-capped
fruit-dove Ptilinopus porphyraceus, a likely seeddisperser, in Samoa. Ridley (1930) mentioned
parrots and pigeons eating A. pavonina, but
these birds are probably seed predators, not
dispersers, of medium or large seeds (see Lambert, 1989). Several long-term studies on diets
of neotropical fruit-eating birds have not
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Table 12.1.
179
Plant families and genera containing mimetic fruits.
Species
Lifeform
Distribution
Cyperaceae
Gahnia
Euphorbiaceae Glochidion
sieberana
sumatranum
Herb
Tree
Mal.–Austr.
Austr.
Euphorbiaceae Margaritaria
spp.
Tree
Leguminosae
Abarema
spp.
Tree
Leguminosae
Abrus
precatorius
Vine
Leguminosae
Acacia
auriculaeformis Tree
Leguminosae
Adenanthera
spp.
Tree
Leguminosae
Archidendron
spp.
Tree
Leguminosae
Leguminosae
Batesia
Erythrina†
floribunda
spp.
Tree
Tree
Leguminosae
Ormosia‡
spp.
Tree
Leguminosae
Pararchidendron
pruinosum
Tree
Leguminosae
Pithecellobium
spp.§
Tree
Leguminosae
Rhynchosia
spp.
Vine
Leguminosae
Liliaceae
Ochnaceae
Sophora
Allium
Brackenridgea
secundiflora
tricoccum
nitida
Tree
Herb
Herb
Ochnaceae
Campylospermum elongatum
Ochnaceae
Ochna
atropurpurea
Herb
Paeoniaceae
Paeonia
spp.
Herb
Sapindaceae
Harpullia
arborea
Tree
Family
Genus
Herb
Secondary
compound*
Colour display
Red seed
Orange-red
seed
Metallic blue
Pan Tropical
capsule
Blue-white
?
NTA
seeds, orange
pod
Red and black
Pan Tropical Alkaloids
seeds
Black seeds,
?
Austr.
brown pod,
yellow funicles
Red or blackAlkaloids
Austr./Asia
red seeds,
/Pacific
orange pod
Black seeds,
Saponin
Indomalay,
orange to red
Austr.
pods
Red seeds
?
NTA
Red or
Alkaloids
Trop./
red/black
Subtrop.
seeds
Red or
Alkaloids
Pan
black/red
Tropical
seeds
Black seeds,
?
Austr.–Mal.
red or orange
pod
Black seeds,
Saponin
Neotrop.
pink pod
Black-red
Pan Tropical ?
seeds
Red seeds
Pan Tropical Alkaloids
Black seeds
North America Alkaloids
Pan Tropical Terpenoids, Black seeds,
red sepals
flavonoids
Black seeds,
?
African
red sepals
Pan Tropical Isoflavonid Black seeds,
red calyx
Black seeds,
Alkaloids
M. Europe
red carpel
Black seeds,
Saponin
Indomalay
yellow capsule
*Secondary
?
Tannin,
terpenoids
Alkaloids
compounds found in fruits (reference list sent upon request to author).
species of Erythrina have black or brownish seeds (see Bruneau, 1996).
‡Some species of Ormosia have black seeds or indehiscent fruits (Rudd, 1965).
§Not all Pithecellobium species have mimetic fruits. Also includes Cojoba.
Mal.–Austr., Malesia–Australasian; NTA, neotropical Americas; M. Europe, middle Europe.
†Several
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Seed Dispersal of Mimetic Fruits
reported consumption of mimetic fruits
(Wheelwright et al., 1984; Loiselle and Blake,
1990; Blake and Loiselle, 1992; Galetti and
Pizo, 1996). In fact, very few published studies
have reported evidence of avian frugivores
consuming seeds of mimetic fruits in the wild
(French, 1990; Quin, 1996; Foster and Delay,
1998).
Mammals may eat mimetic fruits, but are
probably seed predators. For instance, pigtailed macaques (Macaca nemestrina) were
recorded preying upon Ormosia venosa seeds on
the forest floor in Malaysia (Miura et al., 1997).
Peres and van Roosmalen (1996) also recorded
spider monkeys preying upon Ormosia seeds in
an Amazonian forest.
How Did Mimetic Fruits Evolve?
Three Adaptive Hypotheses
The aposematism hypothesis
Aposematism refers to a warning signal
(e.g. colours) of animals to advertise unpleasant attributes to avoid predation (Edmunds,
1974). Foster and Delay (1998) proposed
that the colour of mimetic fruits is a warning
signal of toxicity to seed predators, especially
parrots. Some mimetic species (Ormosia, Abrus,
Sophora) are well known to contain alkaloids
that can kill domestic animals (Tokarnia
and Dobereiner, 1997). Alkaloids in seeds,
however, are not restricted to mimetic
fruits (Herrera, 1982; Cipollini and Levey,
1997).
The seed dispersal system of mimetic fruits is
still controversial and poorly tested. We present experimental tests of three hypotheses,
using Ormosia arborea (Leguminosae, Papilionoidea) as a focal species.
The parasitism hypothesis
Batesian mimicry involves three agents: the
selective agent (the bird), the model (an ornithochoric fruit) and the mimic (the mimetic
fruit). All agents affect each other, but only
the mimic benefits from this relationship
(Endler, 1981). Early studies on seed dispersal
hypothesized that mimetic fruits deceive
seed-dispersers. Because they provide no benefits for the dispersers and, in fact, take advantage of them, the relationship is parasitic.
The mutualism hypothesis
Peres and van Roosmalen (1996) proposed a
hypothesis that mimetic fruits of some species
are ingested by terrestrial granivorous birds
(tinamous, guans and trumpeters) because
the hard-stoned seeds are used as grit to break
down other food in the bird’s gizzard (‘hard
seed for grit’ hypothesis). The abrasive treatment of the mimetic fruits is hypothesized as
essential for their germination. Peres and van
Roosmalen (1996) did not provide any evidence that seeds ingested by terrestrial granivorous birds germinate better than seeds ingested by other birds.
Material and Methods
Plant species
Ormosia spp. are commonly used in studies on
mimetic fruits (McKey, 1975; Peres and van
Roosmalen, 1996; Foster and Delay, 1998).
The genus contains approximately 100 species
that have entirely red, red with a black spot
(bicoloured) or entirely black seeds (Rudd,
1965). It is widely distributed and its taxonomy
is relatively well studied (Rudd, 1965). Apparently all Ormosia species have long fruiting
periods (Peres and van Roosmalen, 1996; Foster and Delay, 1998). Our study species,
O. arborea, occurs in south-east Brazil in forest
and restingas (Rudd, 1965). In some areas,
fruits persist for as long as 36 months
(M. Galetti, unpublished data). The fruit is
a dehiscent pod, exposing a single red
and black seed. Mean seed diameter is
12.85 ± 1.18 mm (n = 20). Because accurate
information on seed-dispersers of O. arborea
is lacking, we combined field and captiveanimal experiments; we assume that experiments with captive animals can provide important clues to the dispersal of O. arborea seeds in
the field.
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Study Areas
All captive experiments were carried out at
Bosque dos Jequitibás Zoo, Campinas, southeast Brazil, and at CRAX, a bird breeding facility specializing in Galliformes, at Contagem,
Minas Gerais.
Field experiments were carried out in
three areas:
1. Bosque dos Jequitibás, a 10 ha forest fragment in Campinas with a high density of agoutis (Dasyprocta leporina).
2. Parque Estadual Intervales, a 50,000 ha
Atlantic Forest site near Sete Barras, São Paulo.
It hosts one of the highest diversities of birds in
the entire Atlantic Forest of Brazil (Aleixo and
Galetti, 1997).
3. Estação Ecológica (EE) de Caetetus in
Gália west of São Paulo. It has 2100 ha of
semideciduous forest, with large populations
of large frugivorous birds and mammals.
What Eats Ormosia Seeds?
Aviary experiments
We first asked: ‘What eats and disperses
O. arborea seeds?’ We offered seeds ad libitum
to several species of captive birds we thought
were likely to consume O. arborea seeds in
the field. These included large frugivores–
granivores (jacutinga, Pipile jacutinga, n = 2
birds; black-legged guan, Penelope obscura,
n = 3; trumpeter, Psophia viridis, n = 2; curassows, Crax fasciolata and Crax blumenbackii,
n = 8 of each; and solitary tinamous, Tinamous
solitarius, n = 8) and large, canopy frugivores
(toco toucan, Ramphastos toco, n = 6; and bellbird, Procnias nudicollis, n = 1).
All birds were housed in large cages and
supplied food (fruits and a synthetic diet)
ad libitum and were in good health. We also
offered O. arborea seeds to several mammal species (spider monkey, Ateles paniscus, n = 2; capuchin monkey, Cebus apella, n = 5; and tapir,
Tapirus terrestris, n = 2) and reptiles (tegu lizard, Tupinambis meriane, n = 5; and tortoise,
Geochelone carbonaria, n = 2) to observe how the
seeds were treated (swallowed, chewed up, spat
181
out, etc.). These experiments provided qualitative data; quantitative data are not presented
because some animals became satiated during
the experiments.
Field experiments
To determine O. arborea consumers in the
field, we watched three fruiting O. arborea trees
for 60 h (30 h during the dry season and 30 h
during the wet season) at EE Caetetus.
Because we did not observe any visitors to
these trees, we set up five camera traps
(Camtrack) to detect frugivores eating
O. arborea seeds on the forest floor. One camera was set up below a fruiting O. arborea for
4 months at Caetetus, while the others were set
up at Parque Estadual Intervales. In total, the
cameras were able to detect visits to the seeds
of O. arborea during 4080 h. All animals that
ate O. arborea seeds in captivity and that were
photographed were assumed to eat O. arborea
in the wild, even though we did not directly
or indirectly (via photography) observe them
ingesting seeds.
Testing the Parasitism Hypothesis:
Do O. arborea Seeds Deceive Avian
Frugivores in the Presence of a
Putative Model?
If mimetic fruits deceive seed-dispersers, we
would expect that birds would not distinguish
between the model (rewarding) fruit and the
mimetic fruit. In neotropical forests, several
plant species produce arillate fruits that may
be models of mimetic fruits. These include
Copaifera langsdorffii, Copaifera trapezifolia
(Leguminosae), Sloanea spp. (Elaeocarpaceae),
Cupania spp. (Sapindaceae), Alchornea triplinervia (Euphorbiaceae) and many others (see
Galetti, 1996). All experiments were carried
out using C. langsdorffii (Leguminosae, Caesalpinoidea) as the model. This bird-dispersed
species has black seeds partially covered by an
orange aril and a diaspore similar in size to
that of O. arborea and is eaten by several bird
species (Galetti and Pizo, 1996).
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Seed Dispersal of Mimetic Fruits
Experiment using adult birds
Three pet wild-caught toucans (R. toco)
and three guans (Penelope superciliaris)
were housed in separate enclosures
(2.5 m × 1.5 m × 1.5 m). Because none was
captive-bred and all came from undetermined
origins, it is possible that these birds had previous contact with O. arborea and its models
before capture. The three toucans were chosen from a group of 15 that were living in a
large enclosure. All experiments started 1
week after the birds were housed in our small
enclosures, which appeared to be sufficient
time for acclimatization. All birds were fed
bananas and papaya and seemed to be in good
health. Feeding trials with birds were conducted in the morning, when the birds were
most active. Two experiments were carried out
on adult birds. In the first, we offered a dish
containing 20 O. arborea and 20 C. langsdorffii
seeds to the three guans and to the three
toucans. After 24 h we counted the number
of seeds of each type ingested and defecated.
After 48 h we repeated the experiment using
the same birds. In the second experiment, we
used only toucans. We offered each toucan
(not all three together, as in the first experiment) 20 O. arborea seeds, 20 C. langsdorffii
fruits (i.e. seed plus aril) and 20 O. arborea
seeds with transplanted C. langsdorffii arils.
After 24 h we counted the number of seeds of
each type ingested and defecated. The experiment was repeated twice (i.e. 60 seeds of each
type were offered to each toucan).
Experiment using naïve birds
Naïve birds are less selective in their diet than
adult birds (Barrows et al., 1980), so we predicted that naïve birds would be more easily
‘deceived’ by mimetic fruits than adult birds.
We tested whether O. arborea seeds would
deceive naïve, captive-born toucans (i.e. if
O. arborea seeds would be ingested by them).
Three captive-bred R. toco were housed in separate enclosures. They were fed their normal
diet and offered 30 O. arborea seeds. We
counted the number of seeds swallowed. After
24 h and 48 h we repeated the experiment.
After another 2 days, without offering any
O. arborea we offered Ormosia seeds with
attached artificial arils made of red plasticine
(without smell or taste). The number and type
of seeds swallowed were recorded after 3 h.
The trials were replicated after 24 and 48 h.
After another 2 days, we offered O. arborea
seeds without arils to determine if the behaviour of the birds had changed.
Field experiments
At EE Caetetus, we placed five stations below
the crown of a fruiting C. langsdorffii tree. The
tree bore thousands of ripe arillate fruits,
which were frequently dropped to the forest
floor by monkeys and birds. Fallen fruits were
avidly consumed by three species of thrushes
(Turdus albicollis, Turdus rufiventris and Turdus
amaurocalinus) and by white-lipped (Tajacu
pecari) and collared peccaries (Tajacu tajacu).
Both peccary species destroy C. langsdorffii
seeds and thus were considered seed
predators.
Stations were spaced 3 m apart. At each
station we placed one O. arborea seed, three
C. langsdorffii seeds with attached arils and one
O. arborea seed with a transplanted C. langsdorffii aril. C. langsdorffii arils can be easily fitted
on to O. arborea seeds in such a way that even
humans cannot distinguish the difference
between O. arborea with C. langsdorffii arils and
C. langsdorffii seeds with C. langsdorffii arils. The
ratio of three model seeds to one mimetic fruit
was arbitrary. The stations were checked every
15 min, the number and type of seeds eaten
recorded and removed seeds replaced. Sixtynine replacements were made during 5 h of
observations.
Testing the Mutualism Hypothesis
(‘Hard Seed for Grit’ Hypothesis): Do
O. arborea Seeds Require Abrasive
Treatment to Germinate?
The ‘hard seed for grit’ hypothesis (Peres
and van Roosmalen, 1996) predicts that seeds
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defecated or regurgitated by birds with
non-muscular gizzards (e.g. toucans) would
have lower germination rates than those
defecated or regurgitated by birds with muscular gizzards (e.g. Galliformes). To test this
prediction, all seeds defecated or regurgitated
by guans (Penelope and Pipile) and toucans
(Ramphastos) in the aviary experiments were
collected and tested for germination in the
greenhouse. Each seed was sown in vermiculite and watered daily. Control seeds were not
defecated or regurgitated but were otherwise
treated identically.
Are Red and Black Seeds More Prone
to be Eaten by Animals than Black
Seeds?
If mimetic fruits of O. arborea evolved their
conspicuously contrasting colours to attract
frugivores, we would predict that red and
black seeds are more likely to be eaten than
totally black seeds.
Aviary experiments
We offered three captive toucans (R. toco) 30
O. arborea seeds and 30 O. arborea seeds painted
completely black with non-toxic black, as
described in the first aviary experiment. The
painted seeds were left to dry for 24 h before
being offered to the birds. We then counted
the number of each seed type ingested and
defecated, 24 h after offering them.
183
frugivore visits to each type of seed (n = 3
cameras).
Testing the Aposematism
Hypothesis: Do the Colours of
O. arborea Seeds Reduce Seed
Predation by Rodents?
Aposematism is a well-studied phenomenon in
insects (e.g. Gamberale and Tullberg, 1998),
in which bright colours have evolved as a
warning display to predators (usually birds)
to reduce the probability of attack (Ritland,
1991). If mimetic fruits evolved colourful
seeds as a warning signal of toxicity to seed
predators, we would expect that black seeds
would be more prone to predation by rodents
than would red and black seeds. Note that
this prediction is the opposite of that generated by the mutualism hypothesis; rather than
focusing on the tendency of brightly coloured
seeds to attract dispersers, it focuses on the
tendency of these seeds to repel seed
predators.
Field experiments
We carried out the experiment in Bosque dos
Jequitibás, where agoutis (Dasyprocta leporina)
are tame and can be observed closely. We set
up 30 stations, spaced 100 m apart. At each station we placed one O. arborea seed (control)
and one O. arborea painted completely black.
We recorded the number and type of seeds
eaten by agoutis after 120 h.
Field experiment
Statistical Analysis
At Parque Estadual Intervales we set up 29
plots for each treatment. One treatment had
20 O. arborea seeds that were painted all black,
the second treatment had 20 O. arborea seeds
in which only the black part of the seed was
painted black (to test whether the ink would
affect seed predation) and the third had 20
O. arborea seeds that were untreated, as controls. Plots were spaced 100 m apart. The number of removed seeds was counted after 40
days. One camera trap was set up to record
Prior to statistical analyses, all variables were
tested for normality and homogeneity of variance. When assumptions of normality and
equal variance were not met, the variables
were transformed (log transformation for
mass and linear dimensions; angular transformations for proportions). If assumptions were
still not met, we used non-parametric tests.
Categorical data were analysed with χ2 tests or,
when expected values were < 5, with G tests
(Sokal and Rohlf, 1995).
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Seed Dispersal of Mimetic Fruits
Results
What eats O. arborea seeds?
Aviary experiments
In trials with captive animals, O. arborea seeds
were occasionally swallowed by a small assemblage of birds, including toucans (R. toco),
guans (P. jacutinga and P. obscura) and trumpeters (P. viridis), but were ignored by bellbirds (P. nudicollis), mammals (T. terrestris,
C. apella, A. paniscus) and reptiles (G. carbonaria and T. meriane). Curassows (C. fasciolata
and C. blumenbackii) mandibulated the seeds
but did not swallow them.
Field observations
In the wild, we observed white-lipped
(T. pecari) and collared peccaries (T. tajacu)
preying upon the seeds of O. arborea at EE
Caetetus. Both peccaries chewed seeds and
spat out the seed-coat. We saw no bird
consume O. arborea seeds during 60 h of
observation.
At Intervales, we recorded in the photographs only agoutis (D. leporina, n = 15 pictures), tinamous (T. solitarius, n = 5) and a dove
(Geotrygon montana, n = 3) visiting the fallen
seeds of O. arborea. Both agoutis and tinamous
were classified as seed predators based on
captive studies.
Testing the parasitism hypothesis:
do O. arborea seeds deceive avian
frugivores in the presence of its putative
model?
Experiment using adult birds
In the first experiment, both toucans and
guans preferred C. langsdorffii fruits to
O. arborea seeds (Mann–Whitney U test, U = 21,
P = 0.002). There was no difference between
their degree of preference (U = 52, P = 0.23).
Only eight seeds of O. arborea were eaten by
toucans and five by guans, compared with 79
and 25 C. langsdorffii fruits consumed by toucans and guans, respectively.
In the second experiment (in which we
offered O. arborea seeds, O. arborea seeds with
aril and C. langsdorffii fruits), there was a statistically significant difference among the three
seed types in the number ingested by toucans
(Kruskal–Wallis test, H = 9.02, P = 0.009). Of
120 presentations, adult toucans ingested
13.2 ± 7.5 C. langsdorffii fruits, 10.7 ± 3.6
O. arborea seeds with aril of Copaifera and only
1.3 ± 3.3 O. arborea seeds.
Experiment using naïve birds
Naïve toucans consumed significantly more
O. arborea seeds when only O. arborea seeds
were offered than did adult, non-naïve
toucans (two-way repeated-measures analysis
of variance (ANOVA), F = 19.90, P < 0.0001).
After ingesting O. arborea seeds with transplanted arils, the toucans rejected bare
O. arborea seeds and even O. arborea seeds with
transplanted arils (Fig. 12.1).
Field experiments
In our field experiment, wild birds (Turdus
spp.) did not ingest any O. arborea seeds. They
ingested only C. langsdorffii fruit (53% of fruits
offered, n = 207 seeds) and O. arborea seeds
with transplanted arils (14% of fruits offered,
n = 69 seeds). The birds strongly preferred
C. langsdorffii fruits to O. arborea seeds with
transplanted aril (G test, G = 16.1, d.f. = 1,
P < 0.0001).
Testing the mutualism hypothesis (‘hard
seed for grit’ hypothesis): do O. arborea
seeds require abrasive treatment to
germinate?
We collected 19 O. arborea seeds from the faeces of P. jacutinga, 20 from P. obscura and four
from P. viridis. Tinamous solitarius ingested a
few seeds, but we did not find any intact in
their faeces. Seeds defecated or regurgitated
by captive guans and toucans and the control
were planted in a greenhouse and compared
(Fig. 12.2).
Eight months after sowing, seeds of
O. arborea started to germinate. After 13
months, there was a significant difference
in per cent germination between treatments
and control (G = 6.4, d.f. = 2, P = 0.04). However, this difference was not the one predicted.
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Fig. 12.1. Mean (and standard deviation) of number of Ormosia arborea seeds eaten by three naïve
toucans (Ramphastos toco). Different letters signify statistical differences (P < 0.05).
Fig. 12.2. Germination rates of Ormosia arborea seeds defecated or regurgitated by three species of
birds and the control seeds, which were not ingested by birds. No seeds germinated for the first 7 months
after sowing; these months are not shown on the x axis.
In particular, there was no difference in per
cent germination among seeds ingested by
guans and toucans and, in fact, all ingested
seeds had substantially lower per cent germination than control seeds (Fig. 12.2).
These results do not support the prediction
that germination of O. arborea seeds is
higher when passed through the gut of
granivorous birds with muscular gizzards
(e.g. guans) than when passed through
frugivorous birds with non-muscular gizzards
(e.g. toucans).
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Seed Dispersal of Mimetic Fruits
Are red and black seeds more prone to be
eaten by animals than black seeds?
deception is extremely rare in the wild (Foster
and Delay, 1998).
Aviary experiments
There was no difference in the number of
natural (red and black) and all-black O. arborea
seeds consumed by toucans (25 all-black seeds
versus 26 red/black seeds). This suggests that
the colour of O. arborea seeds does not
enhance seed ingestion by toucans in these
circumstances. The influence of seed colour
on probability of ingestion may be different in
nature, however.
The mutualism hypothesis
We found no difference in seed predation
levels by agoutis between black-plus-red and
all black seeds (χ2 = 12.4, P = 0.002). Sixtynine per cent of natural O. arborea seeds and
79% of O. arborea seeds painted all black were
preyed upon after 120 h.
The mutualism hypothesis (‘hard seed for
grit’ hypothesis) posits that the hard seeds of
mimetic fruits are dispersed by terrestrial
galliform birds that use the seeds as grit. The
abrasive treatment in the birds’ gut is presumably essential for seed germination (Peres and
van Roosmalen, 1996). Our experiments led
us to reject this hypothesis; we did not find a
difference in seed germination of O. arborea
seeds defecated by birds that would or would
not be likely to use the seeds as grit. In fact, all
seeds from bird defecations had lower germination rates than uningested control seeds.
Moreover, we would expect that the contrasting colours of O. arborea seeds on the forest
floor would attract more dispersers than if
they were only black (as proposed by Peres
and van Roosmalen, 1996). Again, we did not
find any difference in seed removal between
black and red/black seeds. Studies on the
diet of neotropical Galliformes (Cracidae and
Tinamidae) have not reported any species of
mimetic fruit in their diet (Erard et al., 1991;
Galetti et al., 1996; Yumoto, 1999; Santamaria
and Franco, 2000). All large terrestrial cracids
(Crax, Mitu) and tinamids (Tinamous) are
primarily seed predators of large seeds
(Bockerman, 1991; Yumoto, 1999; Santamaria
and Franco, 2000). Jacutingas (Pipile) and
guans (Penelope) are more arboreal and are
mainly seed-dispersers, but they were never
recorded visiting areas with O. arborea seeds by
our cameras.
Discussion
The aposematism hypothesis
The experiments described here comprise the
first attempt to test alternative hypotheses
about mimetic fruits. We caution that the
results of experiments using captive birds are
tentative because we do not know whether the
birds had previous experience with mimetic
fruits in the wild. Overall, our results best
support the parasitism hypothesis – mimetic
fruits deceive avian frugivores – although such
The aposematism hypothesis was also rejected,
at least for large-bodied diurnal rodents
(e.g. agoutis), but more experiments using
other vertebrates, such as parrots, are necessary. Ormosia spp. are rich in quinolizinide
alkaloids (Ricker et al., 1999), which may be
important in deterring seed predation by
rodents and insects (P. Guimarães, M. Galetti
and J. Trigo, unpublished data). Other taxa
Field experiments
We found no statistical difference in removal
of natural O. arborea seeds, O. arborea seeds
painted all black and O. arborea seeds with the
naturally black part painted black (ANOVA,
F = 0.6, d.f. = 2, P = 0.5). Ormosia arborea seeds
that were naturally red and black were
consumed slightly more often (2.3 ± 2.6
seeds) than O. arborea seeds with only the black
part painted (1.9 ± 2.7) and O. arborea seeds
painted completely black (1.4 ± 2.3, n = 190
seeds of each seed type offered).
Testing the aposematism hypothesis:
do the colours of O. arborea seeds
reduce seed predation by rodents?
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with mimetic fruits (e.g. Erythrina, Abrus and
Sophora) are well known to be toxic to vertebrates and insects (Ramos et al., 1999), but
alkaloids are not exclusive to Leguminosae with
brightly coloured seeds (A. Tozzi, 2000,
unpublished data).
The parasitism hypothesis
The only hypothesis supported by our experiments was the parasitism hypothesis. Naïve
birds were more frequently deceived by
O. arborea seeds than were non-naïve birds,
as predicted by the hypothesis. In fact, adult
toucans rejected O. arborea seeds only when
we presented an arillated fruit with a mimetic
fruit. Because mimetic fruits have a long fruiting season, it is likely that mimetic fruits are
more prone to be dispersed during periods of
low fruit availability. Several species considered mimetic have long dormancy and their
seeds can be attached to the pod for up to 3
years (e.g. O. arborea). All of these characteristics are probably adaptations enabling the
plant to maximize the period when seeds
are available to dispersers (Peres and van
Roosmalen, 1996; Foster and Delay, 1998).
Why are Ormosia Seeds Colourful?
Although our experiments support the parasitism hypothesis, we suggest that analysis of
fruit morphology of the entire genus may provide clues to the evolution of colourful seeds.
Fifty species of Ormosia occur in the neotropics
and 50 others in the Old World (Rudd, 1965).
A puzzling aspect of this genus is that even
indehiscent species have colourful seeds and
one dehiscent species has totally black seeds
(Table 12.2). Assuming that species with
187
abiotic dispersal mechanisms and indehiscent
fruits represent the plesiomorphic (ancestral)
state of Papilionoidea (Janson, 1992), we suggest that seed colour cannot be interpreted as
an adaptation to present-day seed-dispersers.
Furthermore, several species of Ormosia
that occur in flooded forests and have indehiscent fruits are dispersed by water (hydrochory) (Ziburski, 1991; Janson, 1992). Therefore, an evolutionary transition between two
passive dispersal modes would be a more parsimonious interpretation than a transition from
hydrochoric to endozoochoric syndromes
(Janson, 1992; Jordano, 1995). In fact, autochory and hydrochory seem to be the main
seed-dispersal syndromes in several mimetic
species. Several species with mimetic fruits
occur along rivers and have been recorded in
studies on water dispersal. Murray (1986) listed
two mimetic species (Abrus precatorius and
Erythrina variegata) as capable of long-distance
dispersal by ocean currents. It seems astonishing that there is no record of birds dispersing
A. precatorius, one of the most invasive plants in
Florida, USA. Adenanthera pavonina is also considered invasive in several islands in Oceania,
but we do not have any unambiguous records
of birds dispersing viable seeds of this species
(only records of gut contents) (Steadman and
Freifeld, 1999).
The current worldwide distribution of
Sophora (which belongs to the same tribe as
Ormosia), another genus with mimetic fruits,
is due to ocean dispersal (Hurr et al., 1999),
although Sophora macrocarpa is also dispersed by
cattle in Chile (R. Bustamante, 2000, personal
communication). Most species of Archidendron
and P. pruinosum, also mimetic species, occur
along watercourses or in coastal areas (Cowan,
1998a, b). Several species of Erythrina occur in
flooded areas and are able to float (Bruneau,
1996) and there are scant observations of
Table 12.2. Seed colour, habitat and occurrence of dehiscent fruits in neotropical Ormosia (following
Rudd, 1965).
Seed colour
Indehiscent
Dehiscent
Habitat
Red
Black
Red/black
Terra firme
Riverine
5
8
0
1
2
34
0
18
5
14
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Seed Dispersal of Mimetic Fruits
Erythrina being dispersed by birds (C.T. Downs,
2000, unpublished data).
Ecological patterns not linked to adaptive
processes from current selection but to phylogenetic constraints may explain the seed colour of some mimetic species. For instance, seed
colour in Erythrina is highly constrained by
phylogeny (Bruneau, 1996). Phylogenetic constraints in several traits of fruit morphology, in
fact, has been found to be more common than
traits moulded by ongoing effects of natural
selection (Herrera, 1987, 1992; Fischer and
Chapman, 1993; Jordano, 1995).
We propose that the seed-dispersal system
of O. arborea, and probably of most Leguminosae
with mimetic fruits, is a typical case of exaptation. Exaptation represents the secondary use
of a trait already present for other (generally
historical) reasons (i.e. traits fit for their
current role but not designed for it) (Gould
and Vrba, 1982). Endozoochorous dispersal
of mimetic fruits may certainly occur, but it is
an extremely rare event. Despite being a rare
event, sporadic dispersal by vertebrates might
greatly contribute to fitness of rare species with
mimetic fruits.
But what constitutes a rare event in vertebrate seed dispersal? There are few long-term
studies on fruit fall to evaluate this question for
mimetic fruits. Data for 13 years (January 1987
to January 2000) of seed fall on Barro Colorado
Island (Panama) revealed only two seeds of
Ormosia (one O. coratti, one O. macrocalyx) away
from conspecifics in 200 0.5 m2 traps (100 m2)
in a 50 ha plot. One seed was found more than
400 m from any Ormosia adult and the other
95 m away (S.J. Wright and R. Condit, 2000,
unpublished data). The long-distance movements of both these Ormosia seeds are probably
the result of arboreal seed dispersal (perhaps
by toucans). In Cameroon, seed-rain samples
from 12 months of trapping (totalling 77.9 m2)
below endozoochoric trees contained only one
Erythrina seed (C. Clark, 2000, unpublished
data). The same pattern was found for P. broteroi in Sierra de Cazorla, Spain. Three years of
data on seed fall (1200 traps) contained only
one record of a dispersed seed, 13 m away from
the nearest Paeonia adult ( J.L. Garcia-Castaño
and P. Jordano, 2000, unpublished data). Likewise, Foster and Delay (1998) reported that, in
85 h of watching Ormosia trees (three species),
only 19 seeds were dispersed away from the
trees and only one was swallowed by birds.
Peres and van Roosmalen (1996) did not
record any arboreal frugivores ingesting
Ormosia lignivalvis in 185 h of focal tree
observations.
However, our findings should not be
taken out of the context of the plants’ demography. In particular, we measured only the
number of seeds dispersed, not seedling establishment. The low frequency of seed dispersal
means either low selection or low reproduction. Several additional issues should be pursued to understand the mimetic fruit-dispersal
system. Would results have been different if the
seeds were black in colour? Would a tree actually have higher fitness if it put a nutritive
reward on its seeds? To what extent does the
maintenance of scarce populations of mimeticfruited species depend on rare events of seed
dispersal by frugivores?
Although mimetic fruits are extremely
difficult to study in the wild, study of their
seed-dispersal systems may be as informative
as the study of more typical fruits and is
paramount for understanding the evolution
of plant–frugivore interactions. The balance
between fruit attraction and chemical defence
may be better understood when both extremes
of the deception–reward gradient are
considered.
Acknowledgements
I am deeply grateful to all students of the Plant
Phenology and Seed Dispersal Research
Group, particularly Liliane Zumstein, Inez
Morato and Paulo Guimarães, Jr, for their
help in the field and aviary experiments and to
Ana Tozzi for enlightening discussions on
Leguminosae phylogeny. I also thank the
administration of Bosque dos Jequitibás in
Campinas and Mr Roberto Azeredo from
CRAX for allowing our trials with their captive
birds. I am grateful to Instituto Florestal and
Fundação Florestal de São Paulo for providing
all facilities at EE Caetetus and Parque Intervales. My thanks also go to C. Clark, J.S. Wright
and J.L. Garcia-Castaño for allowing me to use
their data on seed fall. Daniel Janzen, Pedro
Jordano, Carlos Herrera, Douglas Levey and
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M. Galetti
Marco A. Pizo provided helpful discussion and
helped improve the manuscript. Finally, I
thank FAPESP (Fundação de Ampara a Pesquisa do Estado de São Paulo) (96/10464-7)
and CNPq (Conselho Nacional de Desenvolrimento
Científico
e
Tecnológico)
(300025/97-1) for financial support.
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